Upregulation of bundle sheath electron transport capacity under limiting light in C₄Setaria viridis

Abstract

SUMMARY C4 photosynthesis is a biochemical pathway that operates across mesophyll and bundle sheath (BS) cells to increase CO2 concentration at the site of CO2 fixation. C4 plants benefit from high irradiance but their efficiency decreases under shade, causing a loss of productivity in crop canopies. We investigated shade acclimation responses of Setaria viridis, a model monocot of NADP‐dependent malic enzyme subtype, focussing on cell‐specific electron transport capacity. Plants grown under low light (LL) maintained CO2 assimilation rates similar to high light plants but had an increased chlorophyll and light‐harvesting‐protein content, predominantly in BS cells. Photosystem II (PSII) protein abundance, oxygen‐evolving activity and the PSII/PSI ratio were enhanced in LL BS cells, indicating a higher capacity for linear electron flow. Abundances of PSI, ATP synthase, Cytochrome b6f and the chloroplast NAD(P)H dehydrogenase complex, which constitute the BS cyclic electron flow machinery, were also increased in LL plants. A decline in PEP carboxylase activity in mesophyll cells and a consequent shortage of reducing power in BS chloroplasts were associated with a more oxidised plastoquinone pool in LL plants and the formation of PSII – light‐harvesting complex II supercomplexes with an increased oxygen evolution rate. Our results suggest that the supramolecular composition of PSII in BS cells is adjusted according to the redox state of the plastoquinone pool. This discovery contributes to the understanding of the acclimation of PSII activity in C4 plants and will support the development of strategies for crop improvement, including the engineering of C4 photosynthesis into C3 plants.

Here comes the sun: How optimization of photosynthetic light reactions can boost crop yields

“…This review focuses on the photosynthetic light‐dependent reactions, the optimization of which is relevant to improving both C3 and C4 photosynthesis in plants and photosynthetic micro‐organisms (Leister, 2012; Ruban, 2015; von Caemmerer and Furbank, 2016; Cardona et al, 2018; Simkin et al, 2019; Batista‐Silva et al, 2020; Ermakova et al, 2021b; Sales et al, 2021; Santos‐Merino et al, 2021). Modeling studies have suggested that improving the quantum yield and electron transport capacity have a greater potential for increasing the productivity of crops than other photosynthetic mechanisms, such as improving Rubisco activity (Gu et al, 2014; Yin and Struik, 2015, 2021a; Wu et al, 2019).…”

Increased sedoheptulose-1,7-bisphosphatase content in the C4 species Setaria viridis does not affect photosynthesis

“…S. viridis uses NADPH-dependent malic enzyme (NADP-ME) decarboxylation system in the bundle sheath chloroplast (Fig. 6) and, similar to most of NADP-ME species, S. viridis has low PSII activity and linear electron transport rate in bundle sheath cells (Ermakova et al, 2021a). This prompts export of part of the 3-phosphoglycerate (3-PGA) pool to the mesophyll for conversion to triose phosphate, which then diffuses back to the bundle sheath, known as the triose phosphate shuttle (von Caemmerer and Furbank, 2016 and references therein) (Fig.…”

“…BS strands were isolated following the procedure of Ghannoum et al (2005) as described in detail in Ermakova et al (2021a). RNA was isolated from leaves and BS strands, ground in liquid N 2 , using the RNeasy Plant Mini Kit (Qiagen, Venlo, The Netherlands).…”

Faster responses of photosynthesis to light transitions increase biomass and grain yield in transgenicSorghum bicoloroverexpressing Rieske FeS

“…The vast majority of agriculturally important C4 crops, like maize, sorghum (Sorghum bicolor), sugarcane, miscanthus and several millets (e.g., Setaria italica), belong to the NADP-ME subtype of C4 photosynthesis which employs NADP + -dependent malic enzyme to decarboxylate the C4 acid malate in BS chloroplasts (Furbank, 2011). Because of the drastic differences in biochemistry of mesophyll and BS cells in NADP-ME plants, electron transport chains of the two cell types are also largely different: mesophyll cells predominantly run linear electron flow and BS cells -cyclic electron flow (Ermakova et al, 2021a;Munekage, 2016). To coordinate the production of NADPH and ATP between cells, plants need to tightly regulate the distribution of available light energy (Bellasio and Ermakova, 2021;Bellasio and Lundgren, 2016).…”